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From chemolithoautotrophs to electrolithoautotrophs: CO2 fixation by Fe(II)-oxidizing bacteria coupled with direct uptake of electrons from solid electron sources.

Ishii T, Kawaichi S, Nakagawa H, Hashimoto K, Nakamura R - Front Microbiol (2015)

Bottom Line: At deep-sea vent systems, hydrothermal emissions rich in reductive chemicals replace solar energy as fuels to support microbial carbon assimilation.Site-specific marking of a cytochrome aa3 complex (aa3 complex) and a cytochrome bc1 complex (bc1 complex) in viable cells demonstrated that the electrons taken directly from an electrode are used for O2 reduction via a down-hill pathway, which generates proton motive force that is used for pushing the electrons to NAD(+) through a bc1 complex.Activation of carbon dioxide fixation by a direct electron uptake was also confirmed by the clear potential dependency of cell growth.

View Article: PubMed Central - PubMed

Affiliation: Department of Applied Chemistry, School of Engineering, The University of Tokyo Tokyo, Japan.

ABSTRACT
At deep-sea vent systems, hydrothermal emissions rich in reductive chemicals replace solar energy as fuels to support microbial carbon assimilation. Until recently, all the microbial components at vent systems have been assumed to be fostered by the primary production of chemolithoautotrophs; however, both the laboratory and on-site studies demonstrated electrical current generation at vent systems and have suggested that a portion of microbial carbon assimilation is stimulated by the direct uptake of electrons from electrically conductive minerals. Here we show that chemolithoautotrophic Fe(II)-oxidizing bacterium, Acidithiobacillus ferrooxidans, switches the electron source for carbon assimilation from diffusible Fe(2+) ions to an electrode under the condition that electrical current is the only source of energy and electrons. Site-specific marking of a cytochrome aa3 complex (aa3 complex) and a cytochrome bc1 complex (bc1 complex) in viable cells demonstrated that the electrons taken directly from an electrode are used for O2 reduction via a down-hill pathway, which generates proton motive force that is used for pushing the electrons to NAD(+) through a bc1 complex. Activation of carbon dioxide fixation by a direct electron uptake was also confirmed by the clear potential dependency of cell growth. These results reveal a previously unknown bioenergetic versatility of Fe(II)-oxidizing bacteria to use solid electron sources and will help with understanding carbon assimilation of microbial components living in electronically conductive chimney habitats.

No MeSH data available.


Related in: MedlinePlus

(A) Current vs. time measurements for microbial current generation by Acidithiobacillus ferrooxidans cells on an fluorine-doped tin oxide (FTO) electrode in the absence of Fe2+ ions (solid line) at +0.4 V (vs. SHE). Current vs. time measurements without cells at +0.4 V was also depicted as a reference (broken line) (B) Effects of the deep-UV (254 nm) irradiation to the microbial current generation by the cells in the absence of Fe2+ ions at +0.4 V (solid line). Current vs. time measurements without cells at +0.4 V was also depicted as a reference (broken line). (C)In-situ optical microscope observation of an FTO electrode surface at the indicated time (panel A) after cell inoculation. (D) Plot of microbial current against cell number attached on an electrode surface obtained from in-situ optical microscope observation (panels A and B). The squares of the correlation coefficients were estimated by the addition of the point of origin to the obtained data. The geometric area of the FTO electrode was 3.14 cm2. Initial OD500 was 0.02.
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Figure 1: (A) Current vs. time measurements for microbial current generation by Acidithiobacillus ferrooxidans cells on an fluorine-doped tin oxide (FTO) electrode in the absence of Fe2+ ions (solid line) at +0.4 V (vs. SHE). Current vs. time measurements without cells at +0.4 V was also depicted as a reference (broken line) (B) Effects of the deep-UV (254 nm) irradiation to the microbial current generation by the cells in the absence of Fe2+ ions at +0.4 V (solid line). Current vs. time measurements without cells at +0.4 V was also depicted as a reference (broken line). (C)In-situ optical microscope observation of an FTO electrode surface at the indicated time (panel A) after cell inoculation. (D) Plot of microbial current against cell number attached on an electrode surface obtained from in-situ optical microscope observation (panels A and B). The squares of the correlation coefficients were estimated by the addition of the point of origin to the obtained data. The geometric area of the FTO electrode was 3.14 cm2. Initial OD500 was 0.02.

Mentions: Figure 1A shows current vs. time curves for A. ferrooxidans cultivated in the absence of Fe2+ ions. In the present system, a conducting glass electrode (FTO) poised at +0.4 V (vs. SHE) acts as a sole source of electrons, and dissolved O2 and CO2 are an electron acceptor and a carbon source, respectively. In the absence of bacteria, we detected no electrical current generation (broken line, Figure 1A). On the other hand, in the reactors containing cells, the cathodic current gradually increased to approximately 7 μA after 20 h of cultivation (solid line, Figure 1A). The marked difference in current density depending on the presence of cells indicates that the cathodic current was derived from the metabolic activity of cells. Furthermore, in-situ sterilization of cells with the deep-UV (254 nm) irradiation immediately suppressed the cathodic current generation (Figure 1B). Almost no electrical response was observed after 6 h of sterilization, confirming the strong coupling of metabolic activity to electrical current generation.


From chemolithoautotrophs to electrolithoautotrophs: CO2 fixation by Fe(II)-oxidizing bacteria coupled with direct uptake of electrons from solid electron sources.

Ishii T, Kawaichi S, Nakagawa H, Hashimoto K, Nakamura R - Front Microbiol (2015)

(A) Current vs. time measurements for microbial current generation by Acidithiobacillus ferrooxidans cells on an fluorine-doped tin oxide (FTO) electrode in the absence of Fe2+ ions (solid line) at +0.4 V (vs. SHE). Current vs. time measurements without cells at +0.4 V was also depicted as a reference (broken line) (B) Effects of the deep-UV (254 nm) irradiation to the microbial current generation by the cells in the absence of Fe2+ ions at +0.4 V (solid line). Current vs. time measurements without cells at +0.4 V was also depicted as a reference (broken line). (C)In-situ optical microscope observation of an FTO electrode surface at the indicated time (panel A) after cell inoculation. (D) Plot of microbial current against cell number attached on an electrode surface obtained from in-situ optical microscope observation (panels A and B). The squares of the correlation coefficients were estimated by the addition of the point of origin to the obtained data. The geometric area of the FTO electrode was 3.14 cm2. Initial OD500 was 0.02.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4593280&req=5

Figure 1: (A) Current vs. time measurements for microbial current generation by Acidithiobacillus ferrooxidans cells on an fluorine-doped tin oxide (FTO) electrode in the absence of Fe2+ ions (solid line) at +0.4 V (vs. SHE). Current vs. time measurements without cells at +0.4 V was also depicted as a reference (broken line) (B) Effects of the deep-UV (254 nm) irradiation to the microbial current generation by the cells in the absence of Fe2+ ions at +0.4 V (solid line). Current vs. time measurements without cells at +0.4 V was also depicted as a reference (broken line). (C)In-situ optical microscope observation of an FTO electrode surface at the indicated time (panel A) after cell inoculation. (D) Plot of microbial current against cell number attached on an electrode surface obtained from in-situ optical microscope observation (panels A and B). The squares of the correlation coefficients were estimated by the addition of the point of origin to the obtained data. The geometric area of the FTO electrode was 3.14 cm2. Initial OD500 was 0.02.
Mentions: Figure 1A shows current vs. time curves for A. ferrooxidans cultivated in the absence of Fe2+ ions. In the present system, a conducting glass electrode (FTO) poised at +0.4 V (vs. SHE) acts as a sole source of electrons, and dissolved O2 and CO2 are an electron acceptor and a carbon source, respectively. In the absence of bacteria, we detected no electrical current generation (broken line, Figure 1A). On the other hand, in the reactors containing cells, the cathodic current gradually increased to approximately 7 μA after 20 h of cultivation (solid line, Figure 1A). The marked difference in current density depending on the presence of cells indicates that the cathodic current was derived from the metabolic activity of cells. Furthermore, in-situ sterilization of cells with the deep-UV (254 nm) irradiation immediately suppressed the cathodic current generation (Figure 1B). Almost no electrical response was observed after 6 h of sterilization, confirming the strong coupling of metabolic activity to electrical current generation.

Bottom Line: At deep-sea vent systems, hydrothermal emissions rich in reductive chemicals replace solar energy as fuels to support microbial carbon assimilation.Site-specific marking of a cytochrome aa3 complex (aa3 complex) and a cytochrome bc1 complex (bc1 complex) in viable cells demonstrated that the electrons taken directly from an electrode are used for O2 reduction via a down-hill pathway, which generates proton motive force that is used for pushing the electrons to NAD(+) through a bc1 complex.Activation of carbon dioxide fixation by a direct electron uptake was also confirmed by the clear potential dependency of cell growth.

View Article: PubMed Central - PubMed

Affiliation: Department of Applied Chemistry, School of Engineering, The University of Tokyo Tokyo, Japan.

ABSTRACT
At deep-sea vent systems, hydrothermal emissions rich in reductive chemicals replace solar energy as fuels to support microbial carbon assimilation. Until recently, all the microbial components at vent systems have been assumed to be fostered by the primary production of chemolithoautotrophs; however, both the laboratory and on-site studies demonstrated electrical current generation at vent systems and have suggested that a portion of microbial carbon assimilation is stimulated by the direct uptake of electrons from electrically conductive minerals. Here we show that chemolithoautotrophic Fe(II)-oxidizing bacterium, Acidithiobacillus ferrooxidans, switches the electron source for carbon assimilation from diffusible Fe(2+) ions to an electrode under the condition that electrical current is the only source of energy and electrons. Site-specific marking of a cytochrome aa3 complex (aa3 complex) and a cytochrome bc1 complex (bc1 complex) in viable cells demonstrated that the electrons taken directly from an electrode are used for O2 reduction via a down-hill pathway, which generates proton motive force that is used for pushing the electrons to NAD(+) through a bc1 complex. Activation of carbon dioxide fixation by a direct electron uptake was also confirmed by the clear potential dependency of cell growth. These results reveal a previously unknown bioenergetic versatility of Fe(II)-oxidizing bacteria to use solid electron sources and will help with understanding carbon assimilation of microbial components living in electronically conductive chimney habitats.

No MeSH data available.


Related in: MedlinePlus